Superresolution imaging reveals structurally distinct periodic patterns of chromatin along pachytene chromosomes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 47, 2015, Pages 14635-14640

  Prakash, Kirti ^a,b   Fournier, David ^a   Redl, Stefan ^a   Best, Gerrit ^c   Borsos, Máté ^a,d   Tiwari, Vijay K ^a   Tachibana Konwalski, Kikuë ^d   Ketting, René F ^a   Parekh, Sapun H ^c   Cremer, Christoph ^a,b   Birk, Udo J ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY IMB   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c MAX PLANCK INSTITUTE FOR POLYMER RESEARCH   (Germany)

^d ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

Author keywords

Chromatin organization; Epigenetics; Histone modifications; Meiosis; Superresolution microscopy

Indexed keywords

HISTONE H3; NANOMATERIAL; CHROMATIN; HISTONE; LYSINE;

ANIMAL CELL; CENTROMERE; CHROMATIN STRUCTURE; CONFERENCE PAPER; EMBRYO; FEMALE; GENOME ANALYSIS; HISTONE METHYLATION; MEIOSIS; MICROSCOPY; MOUSE; NONHUMAN; PACHYTENE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; SINGLE MOLECULE LOCALIZATION MICROSCOPY; SUPERRESOLUTION MICROSCOPY; TELOMERE; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; CHROMATIN; CHROMOSOME; GENETIC TRANSCRIPTION; METABOLISM; METHYLATION; PROCEDURES; SYNAPTONEMAL COMPLEX;

ANIMALS; CENTROMERE; CHROMATIN; CHROMOSOMES, MAMMALIAN; HISTONES; LYSINE; METHYLATION; MICE; MICROSCOPY; MODELS, BIOLOGICAL; PACHYTENE STAGE; SYNAPTONEMAL COMPLEX; TRANSCRIPTION, GENETIC;

EID: 84948389136     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1516928112     Document Type: Article

References (40)

1. Baudat F, Imai Y, de Massy B (2013) Meiotic recombination in mammals: Localization and regulation. Nat Rev Genet 14(11):794-806.
2. Cook PR (1997) The transcriptional basis of chromosome pairing. J Cell Sci 110(Pt9):1033-1040.
3. Handel MA, Schimenti JC (2010) Genetics of mammalian meiosis: Regulation, dynamics and impact on fertility. Nat Rev Genet 11(2):124-136.
4. Kim KP, etal. (2010) Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 143(6):924-937.
5. Moens PB, et al. (2002) The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination. J Cell Sci 115(Pt 8):1611-1622.
6. Plug AW, Xu J, Reddy G, Golub EI, Ashley T (1996) Presynaptic association of Rad51 protein with selected sites in meiotic chromatin. Proc Natl Acad Sci USA 93(12):5920-5924.
7. Tease C, Hartshorne GM, Hultén MA (2002) Patterns of meiotic recombination in human fetal oocytes. Am J Hum Genet 70(6):1469-1479.
8. Bell O, Tiwari VK, Thomä NH, Schübeler D (2011) Determinants and dynamics of genome accessibility. Nat Rev Genet 12(8):554-564.
9. Cremer T, et al. (2015) The 4D nucleome: Evidence for a dynamic nuclear landscape based on co-aligned active and inactive nuclear compartments. FEBS Lett 589(20 Pt A):2931-2943.
10. Baudat F, et al. (2010) PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327(5967):836-840.
11. Yamada T, Ohta K (2013) Initiation of meiotic recombination in chromatin structure. J Biochem 154(2):107-114.
12. Buard J, Barthès P, Grey C, de Massy B (2009) Distinct histone modifications define initiation and repair of meiotic recombination in the mouse. EM BO J 28(17):2616-2624.
13. Hernández-Hernández A, et al. (2010) Synaptonemal complex stability depends on repressive histone marks of the lateral element-associated repeat sequences. Chromosoma 119(1):41-58.
14. Cremer C, Masters BR (2013) Resolution enhancement techniques in microscopy. Eur Phys J H 38(3):281-344.
15. Betzig E, et al. (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313(5793):1642-1645.
16. Hess ST, Girirajan TP, Mason MD (2006) Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys J 91(11):4258-4272.
17. Rust MJ, Bates M, Zhuang X (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3(10):793-795.
18. Szczurek AT, et al. (2014) Single molecule localization microscopy of the distribution of chromatin using Hoechst and DAPI fluorescent probes. Nucleus 5(4):331-340.
19. ™ Violet fluorescent probe: A new approach to study nuclear nanostructure at single molecule resolution. Exp Cell Res, 10.1016/j.yexcr.2015.08.020.
20. Lemmer P, et al. (2008) Spdm: Light microscopy with single-molecule resolution at the nanoscale. Appl Phys B 93(1):1-12.
21. Reymann J, et al. (2008) High-precision structural analysis of subnuclear complexes in fixed and live cells via spatially modulated illumination (SMI) microscopy. Chromosome Res 16(3):367-382.
22. Nieuwenhuizen RP, et al. (2013) Measuring image resolution in optical nanoscopy. Nat Methods 10(6):557-562.
23. Montrose J (1968) Synaptinemal complex. Annu Rev Genet 2(1):363-412.
24. Westergaard M, von Wettstein D (1972) The synaptinemal complex. Annu Rev Genet 6(1):71-110.
25. Fraune J, Schramm S, Alsheimer M, Benavente R (2012) The mammalian synaptonemal complex: Protein components, assembly and role in meiotic recombination. Exp Cell Res 318(12):1340-1346.
26. Schücker K, Holm T, Franke C, Sauer M, Benavente R (2015) Elucidation of synaptonemal complex organization by super-resolution imaging with isotropic resolution. Proc Natl Acad Sci USA 112(7):2029-2033.
27. Bisig CG, et al. (2012) Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes. PLoS Genet 8(6):e1002701.
28. Rattner JB, Goldsmith M, Hamkalo BA (1980) Chromatin organization during meiotic prophase of Bombyx mori. Chromosoma 79(2):215-224.
29. Bohn M, et al. (2010) Localization microscopy reveals expression-dependent parameters of chromatin nanostructure. Biophys J 99(5):1358-1367.
30. Syrjänen JL, Pellegrini L, Davies OR (2014) A molecular model for the role of SYCP3 in meiotic chromosome organisation. eLife 3:e02963.
31. Kauppi L, et al. (2011) Distinct properties of the XY pseudoautosomal region crucial for male meiosis. Science 331(6019):916-920.
32. Revenkova E, et al. (2004) Cohesin SMC1 β is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination. Nat Cell Biol 6(6):555-562.
33. Pauler FM, et al. (2009) H3K27me3 forms BLOCs over silent genes and intergenic regions and specifies a histone banding pattern on a mouse autosomal chromosome. Genome Res 19(2):221-233.
34. Zamudio N, et al. (2015) DNA methylation restrains transposons from adopting a chromatin signature permissive for meiotic recombination. Genes Dev 29(12):1256-1270.
35. Spangenberg VE, Ya Dadashev S, Matveevsky SN, Kolomiets OL, Yu F (2010) [How do chromosomes attach to synaptonemal complexes?] Russ J Genet 46(10):1203-1205. Russian.
36. Susiarjo M, Rubio C, Hunt P (2009) Analyzing mammalian female meiosis. Meiosis, ed Keeney S (Springer, Clifton, NJ), pp 339-354.
37. Grull F, Kirchgessner M, Kaufmann R, Hausmann M, Kebschull U (2011) Accelerating image analysis for localization microscopy with FPGAs. 2011 International Conference on Field Programmable Logic and Applications (FPL) (IEEE, Chania, Greece), pp 1-5.
38. Kaufmann R, et al. (2012) Visualization and quantitative analysis of reconstituted tight junctions using localization microscopy. PLoS One 7(2):e31128.
39. Liu J, Li W, Tian Y (1991) Automatic thresholding of gray-level pictures using twodimension Otsu method. 1991 International Conference on Circuits and Systems (IEEE, Shenzhen, China), pp 325-327.
40. George EP, Jenkins GM, Reinsel GC (2008) Time Series Analysis: Forecasting and Control (Wiley, Hoboken, NJ), 4th Ed.